International Oaks

The Journal of the International Oak Society

… the hybrid oak

that time forgot, oak-rod baskets,

pros and cons of grafting…

Issue No. 25/ 2014 / ISSN 1941-2061

 Sudden Oak Death, Phytophthora ramorum:

a Persistent Threat to Oaks

and Other Tree Species

Susan J. Frankel, Plant Pathologist, Katharine M. Palmieri, Public Information Officer

USDA Forest Service, Pacific Southwest Research Station, California Oak Mortality Task Force and California

800 Buchanan Street Forest Pest Council

Albany, CA 94710, USA University of California Cooperative Extension

sfrankel@fs.fed.us Berkeley, CA, 94720, USA

kpalmieri@berkeley.edu

ABSTRACT

This paper reviews the status and management of sudden oak death and sudden larch
death in the urban and wildland forests of California, Oregon, and the United Kingdom. The
causal pathogen, Phytophthora ramorum (Werres, De Cock & Man in’t Veld), was discovered
in all three locations over a decade ago. Despite professional, dedicated attempts, efforts
to contain and eliminate infestations have been unsuccessful. These less than satisfactory
management intervention outcomes underscore the importance of prevention, for once forest
pathogens become established, response is costly and difficult, and eradication is unlikely.
New approaches are needed to protect forests from invasive pathogens.

Keywords: Notholithocarpus densiflorus, Quercus agrifolia, Larix kaempferi, invasive

forest pathogens, forestry management
43
Introduction
Over the past 20 years, Phytophthora ramorum (Werres, De Cock & Man in’t Veld),
the pathogen known to cause sudden oak death, has killed well over 5 million trees along
the coast of California and Oregon as well as millions of Japanese larch trees throughout
much of the United Kingdom (UK) and areas of the Republic of Ireland. Despite
eradication attempts and quarantines, four pathogen strains continue to move undetected
overseas and across continents on nursery plant shipments (Goss et al., 2009; Grunwald
et al., 2012). Meanwhile, in coastal California and Oregon, communities struggle to
remove hazardous snags and reduce fuel loads as they lose tanoak (Notholithocarpus
densiflorus (Hook. & Arn.) Manos, Cannon & S.H. Oh) and coast live oak (Quercus
agrifolia Née) (Frankel, 2008). Additionally, in the UK, commercial Japanese larch
(Larix kaempferi (Lamb.) Carrière) plantations are being clear-cut by the millions to
comply with quarantine regulations and to slow pathogen spread (Brasier and Webber,
2010).
Sudden oak death is emblematic of the threat invasive species pose not only to
oaks, but to the health of forest ecosystems. Here we present a review of the status and
management of sudden oak death in the urban and wildland forests of California and
Oregon and sudden larch death in the UK. In all three locations, determined, skillful
efforts to eradicate or slow pathogen spread have not been fully realized; consequently,
forests and the susceptible trees within them remain threatened. The less than satisfactory

1/ Chlamydospore of Phytophthora ramorum germinating on agar medium and forming a sporangium.

44 International Oaks, No. 25, 2014

 Sudden Oak Death

outcomes of management interventions underscore the importance of prevention, for once

forest pathogens become established, response is costly and difficult, and eradication is
unlikely.

Background
The pattern of mortality and symptoms of sudden oak death were first described in the
mid-1990s (Rizzo et al., 2002), with P. ramorum identified as the causal agent several years
later (Werres et al., 2001). A microscopic, fungus-like organism (Kingdom Stramenopila;
phylum Oomycota) (Photo 1), the biology, genetics, and history of P. ramorum have been
reviewed by Rizzo and Garbelotto (2003), Sansford et al. (2009), Kliejunas (2010), and
Grunwald et al. (2008, 2012). The pathogen is currently known to infect over 135 plant
species, with symptoms including leaf spots and/or twig dieback (USDA APHIS 2012)
on all foliar or ramorum blight hosts and bleeding cankers and/or mortality on all sudden
oak death or sudden larch death hosts, including coast live oak, California black oak (Q.
kelloggii Newberry), Shreve oak (Q. parvula Greene var. shrevei (C.H. Mull.) Nixon),
canyon live oak (Q. chrysolepis Liebm.), tanoak, and Japanese larch. With ramorum
blight affecting common horticultural plants such as rhododendrons and camellias, the
pathogen is able to inadvertently travel long distances via the movement of nursery stock
(Ivors et al., 2006).
Once established in a susceptible forest, pathogen spread can occur through wind-
driven rain, infested soil splash, watercourse currents, or by harvest and transport of
infected plant material (Davidson et al., 2005). Cyclical in nature, the pathogen thrives in
wet conditions, allowing inoculum build up and spread in years with ample moisture. Once
a sudden oak death-susceptible tree is infected, its vascular system becomes obstructed,
frequently leading to the death of the tree within a few years, when dry conditions lead
to high evaporative demands (Brown and Brasier, 2007; Parke et al., 2007). However,
not all infected trees die. Some oaks are able to form cankers that wall off and isolate the
infection (Swiecki and Bernhardt, 2010).
An internationally recognized threat to forest ecosystems and the ornamental plant
trade, P. ramorum quarantines have been initiated in Canada (2001), South Korea (2001),
the US (2002), the UK (2002), Australia (2002), the EU (2002), the Czech Republic
(2003), Taiwan (2006), New Zealand (2006), China (2008), and more than 65 other
countries (COMTF, 2013; Sansford et al., 2009).
In the US, P. ramorum was detected at over 540 wholesale and retail nurseries between
2001 to 2013, with an average of 28 detections per year since 2007 (USDA APHIS,
2013). Detections for P. ramorum in the UK have averaged 50 sites per year from 2004
to 2013 in retail nurseries, garden centers, and plant passport nurseries. The average for
the past seven years has been 37 sites per year (Jane Barbrook, personal communication,
November 26, 2013).

Continental and global movement

Genetic analysis demonstrates that P. ramorum has moved across at least one ocean,
become established, and infected native vegetation at least five times in North America
and Europe (Grünwald et al., 2012; Van Poucke et al., 2012), with four clonal lineages
having been identified in one or more locations. Each lineage (EU1, EU2, NA1, and
International Oaks, No. 25, 2014 45
NA2) is named after the continent where it was first detected, followed by the number
representing its order of discovery on that continent (Grünwald et al., 2009; Van Poucke
et al., 2012).
The NA1 lineage was introduced to North America from an unknown location via
imported nursery stock shipped to a nursery near Santa Cruz, CA sometime prior to
the 1990s (Mascheretti et al., 2008, 2009; Grünwald et al., 2012). In 2004, millions of
camellias potentially infected with the NA1 lineage were inadvertently shipped from a
Los Angeles County, CA nursery to more than 1,200 nurseries in 39 states. The pathogen
was ultimately recovered from 171 nurseries in 21 states (USDA APHIS 2013), and
eventually detected in soil and water adjacent to infested nurseries in Alabama, Florida,
Georgia, Mississippi, North Carolina, Washington, (Oak et al., 2013), Texas (COMTF
2013), and New York (Snover-Clift et al., 2013).
The NA2 lineage has been recovered from nurseries in Washington, California, and
British Columbia, Canada as well as from waterways adjacent to infested nurseries in
Washington and California. In spring 2009, runoff from a Pierce County, Washington
retail nursery was the source of inoculum for salal (Gaultheria shallon Pursh) plants
along a drainage ditch that became infected with the NA2 strain. The plants were
destroyed and the pathogen has since only been recovered from the water in the drainage
ditch (Chastagner et al., 2013).
The EU1 lineage was first detected in nurseries and established gardens in Germany
and the Netherlands on Rhododendron and Viburnum in the 1990s (Werres et al., 2001).
It was then discovered in the UK on Viburnum in 2002 (Lane et al., 2002) and on trees
(Q. falcata Michx.) in 2003 in Sussex, southern Britain (Brasier et al., 2004) as well as in
the Netherlands (Q. rubra L.). It continued to spread throughout the UK, sporulating on
R. ponticum L. and threatening natural heathlands (Walters et al., 2009). Then, in 2009,
Japanese larch emerged in the UK as a new host that both facilitated pathogen spread and
died from infection (Brasier and Webber, 2010). The EU1 lineage has also been recovered
from nurseries and adjacent waterways in California and Washington (COMTF, 2013).
The EU2 strain was first introduced to Northern Ireland and western Scotland in 2007
from Japanese larch, Q. robur L., Vaccinium myrtillus, L., and R. ponticum. Genetic
analysis indicates it is a recent introduction, despite quarantine measures to prevent
pathogen spread (Van Poucke et al., 2012).

Pathogen status in California

Sudden oak death continues to be the primary cause of tree mortality along 600
kilometers/373 miles of the California coast from Monterey County north to Humboldt
County (Figure 1, Photo 2). Infestations occur in densely populated residential areas in
several San Francisco Bay Area counties and in managed and unmanaged woodlands.
The infestation is patchy and, due to an affinity for moisture, limited to areas within 80
kilometers/50 miles of the Pacific Ocean. Aerial surveys identified over 294,000 trees
killed in 2013 alone, a number similar to mortality levels in 2012 (COMTF, 2013). In
California, most of the mortality occurs in coastal evergreen forests with Q. agrifolia,
California bay laurel (Umbellularia californica (Hook. & Arn.) Nutt.), California black
oak, Pacific madrone (Arbutus menziesii Pursh), and other species and in coast redwood
(Sequoia sempervirens (Lamb. ex D. Don) Endl.) forests with tanoak in the understory
(Rizzo et al., 2002).

46 International Oaks, No. 25, 2014

 Sudden Oak Death

2/ Tanoaks killed by sudden oak death near Big Sur, Monterey Co., 2012.

Tanoak is the most susceptible species in California and Oregon. Some local populations
in the Big Sur area (Monterey County, CA) have lost most of their mature tanoak trees
because of sudden oak death (Cobb et al., 2012). Measurements in forest research plots
in Marin County from 2000-2008 found approximately 78% (cumulatively) of all tanoak
to be symptomatic, with a 51% mortality rate, while the cumulative infected rate for
coast live oak was 50% with 32% mortality (McPherson et al., 2005; 2010). Swiecki
and Bernhardt (2013) recorded cumulative mortality of coast live oak at 32% and tanoak
mortality at 54% in Marin, Sonoma, and Napa County plots measured from 2000 to 2012.
In all studies, the mortality rate for both species increased with tree size (McPherson et
al., 2010; Cobb et al., 2012; 2013). Shreve oak, California black oak, canyon live oak,
and Pacific madrone can also be killed by P. ramorum (Swiecki et al., 2013); however,
as these species are not as common in infested areas, data on mortality rates is limited.
Despite widespread infestation throughout California’s 14 infested counties, less than
10% of the native range of tanoak has been infected (Meentemeyer et al., 2012); however,
mortality is expected to continue as the pathogen spreads north into the cool, moist
environments of Northern California and coastal Oregon (Meentemeyer et al., 2011).

International Oaks, No. 25, 2014 47

 OREGON

Humboldt

Mendocino

A Confirmed isolatlon of Phytophthora

ramorum *
Host species for Phytophthora ramorum *"'

<'<- Counties with Phytophthora ramorum

L.-/ confirmed In wlldland
0 Counties with either no data or that currently
have no recorded confirmed cases of
Phytophthora ramorum In wildland
• Oata provided by COFA and UC Davis/UC Berkeley
pathologists
"* California host data from CAL GAP Analysis Project.
Oregon host data from OR GAP Analysis Project. Oata
has been queried to only show the geographic range for
species that are hosts for Phytophthora ramorum.
Note:
- Sampling is occurring throughout the state.
- Nursery confirmations are not depicted.

Figure 1/ Distribution of Phytophthora ramorum in California as of September 30, 2013. (Maggi Kelly,
UC Berkeley, Geospatial Innovation Facility.)

48 International Oaks, No. 25, 2014

 Sudden Oak Death

Management in California
Widely dispersed in California by the time of its discovery in 2000 (Rizzo et al.,
2002), sudden oak death management in the state has been focused on maintaining a
safe environment, minimizing pathogen impacts in infested communities, and preventing
long-distance movement of the pathogen (Frankel, 2008). Management is primarily
locally driven, with landowners (individually or collaboratively) taking action in an
effort to protect resources (Alexander and Lee, 2010). The non-profit California Oak
Mortality Task Force (www.suddenoakdeath.org) works to coordinate sudden oak death-
related activities as well as to provide educational outreach to impacted communities and
industries, lawmakers, land managers, regulators, Native American tribes, and the media.
As the state does not fund or require eradication, most management activity targets
protecting individual high-value and/or high-risk trees, reducing roadside hazards from
dead and failing trees, and abating fuels for fire prevention.
In 2011, an isolated outbreak 80 km/50 mi north of the nearest known California
infestation was identified in Redwood Valley (Humboldt County, CA) and has been
under eradication ever since. The infestation extended across more than 20 properties and
included a mix of residential landholdings as well as large, private timberlands. Over 150
hectares/371 acres were treated with herbicide or by removal of infected trees and adjacent
asymptomatic trees to create a 100 m/328 ft buffer. The multi-agency collaborative
effort, led by University of California Cooperative Extension (UCCE), Humboldt and
Del Norte Counties, relied on early detection and rapid response as the cornerstone of
the eradication effort (Valachovic et al., 2013). However, despite treatment, wet springs
led to pathogen spread into steep, rocky, densely vegetated terrain surrounding infested
properties, which ultimately overwhelmed treatment efforts. As a result, the program is
currently transitioning from eradication to a slow-the-spread or containment program.
The pathogen continues to spread northward, threatening Redwood National and State
Park as well as Yurok, Hoopa, and Karuk tribal lands.

Management in Oregon
In July 2001, P. ramorum was discovered in Curry County, Oregon. Since then it has
spread across public and private lands in forests dominated by tanoak, with Douglas-
fir (Pseudotsuga menziesii (Mirb.) Franco) and other tree species (Goheen et al., 2002;
Hansen et al., 2008). A multi-agency team set out to eradicate the pathogen, with the
state mandating that all infected trees as well as those within a 100 m/328 ft buffer be
cut, piled, and burned on commercial timber lands, residential lots, parks, and federally
managed forests. Although there was no direct cost to landowners, no compensation was
made for loss of timber or other assets (Kanaskie et al., 2013).
Eradication sites were identified using fixed-wing airplanes and helicopters or by water
baiting with native rhododendron and tanoak leaves (Sutton et al., 2009). These surveys
were conducted by the Oregon Department of Forestry (ODF), Oregon State University,
and Oregon Department of Agriculture in cooperation with the USDA Forest Service,
and were followed by ground checks to confirm pathogen presence and identify newly
infected trees for treatment (Kanaskie et al., 2013).
Over $10 million was expended from 2001 to 2012 to eradicate the pathogen in Oregon
(Kanaskie et al., 2013) through a combination of federal and state funds. However,
International Oaks, No. 25, 2014 49
 SUDDEN OAK DEATH
QUARANTINE AREA
DECEMBER 1, 2013

LL-.
,_

0 INFECTED TREE. 2013

• • •. QUARANTINE. 2013
~ GENERAUY INFESTED.AREA
BLMLAND
1
- USFSLANO

Figure 2/ Location of sites infested with Phytophthora ramorum in southwest Oregon that were
discovered in 2013 (as of December 1). Sites enlarged for visibility. (Kanaskie, Oregon Department of
Forestry.)
50 International Oaks, No. 25, 2014
 Sudden Oak Death

3/ Sudden oak death tanoak mortality near Brookings, Oregon inside the “Generally Infested Area” on
private lands that are no longer under state-mandated eradication.

expansion and intensification of disease in late 2012 overwhelmed the funds and
manpower required for treatment, making eradication unachievable. During the 10-year
eradication effort, the pathogen spread from the initial infestation southward, 1.9 km/1.2
mi, and northward and eastward, 28 km/17.4 mi and 7.6 km/4.7 mi, respectively. The area
under quarantine had expanded from 22 km2/8.5 mi2 in 2001 to over 680 km2/263 mi2 in
2013 (Figure 2). Eradication treatments eliminated the pathogen from 39% of the treated
areas (Goheen et al., 2013), yet P. ramorum continued to slowly spread (predominantly
northward, in the direction of storm tracks). Oregon revised its quarantine rule in March
2013, establishing a 125 km2/48 mi2 “Generally Infested Area” (GIA) where eradication
is no longer required. Federal agencies continue to treat infestations on federal lands, but
have redirected funds on private lands to focus on the leading edges of the infestation
in an effort to slow disease spread and eradicate new, high-risk infestations. In the GIA,
concern continues to grow over increased tree mortality posing hazardous conditions to
people, dwellings, and roadways if standing dead trees and fuels are not removed (Photo
3).
Despite continued pathogen spread and disease intensification, Oregon’s program
has had numerous benefits. In the 12 years since the first detection, P. ramorum is still
confined to a relatively small area of Curry County, OR, particularly when compared
to similar areas in California that have only been managed for disease containment and

International Oaks, No. 25, 2014 51

slow-the-spread programs over the same period of time. This containment has protected
wildlife and millions of tanoaks as well as shielded the Oregon nursery, forestry, and
special products industries from quarantine restrictions.

Management in the United Kingdom

In 2002, a P. ramorum quarantine was initiated in England and Wales, limiting imports
of host plants from California and Oregon as a precautionary measure whilst more
evidence was gathered on pathogen risk (Sansford et al., 2010). At about the same time,
the first UK P. ramorum find occurred on Viburnum at a garden center in Sussex, Britain
(Lane et al., 2002). The pathogen continued to be intercepted in nurseries and historic
gardens. From 2004 to 2013, approximately 446 retail and nursery confirmations were
reported in England and Wales (Jane Barbrook, personal communication, November 26,
2013).
In spring 2009, a five year Phytophthora Disease Management Programme was launched
by the UK Food Environment Research Agency (Fera) and the UK Forestry Commission
(Walters et al., 2009). The program expanded research, education, and disease control
through clearance of host plants in high-risk areas, with the goal of reducing inoculum
to epidemiologically insignificant levels through the elimination of sporulating hosts
(primarily R. ponticum). Then, in the summer of 2009 in Southwest England, Japanese
larch was found to be a host of P. ramorum, supporting prolific pathogen sporulation as
well as experiencing extensive dieback and mortality upon infection (Brasier and Webber,
2010). In 2010, P. ramorum was again isolated from larch plantations in Southern Wales,
Northern Ireland, and the Republic of Ireland, and in 2011, it was found in Western
Scotland (Schlenzig and Cooke, 2013). These infestations were the first widespread
instances of lethal damage caused by P. ramorum to a commercially important conifer
species anywhere in the world. In response to the larch detection, statutory Plant Health
Notices were issued to woodland owners, requiring infected trees to be felled. Some
financial assistance was offered through grants (UK Forestry Commission, 2012).
The impacts of the pathogen in the UK include the felling of millions of Japanese
larch in commercial timber plantations, removing highly-valued rhododendron plants
in historic gardens to maintain phytosanitary conditions, and costly impacts to the
nursery industry for regulatory compliance (Sandsford et al., 2009). P. ramorum has also
been found infecting bilberry, or European blueberry (V. myrtillus L.) (FERA 2012), in
valuable, native lowland and upland heathlands.
Aerial surveys in spring 2013 detected a major disease expansion in the Dumfries and
Galloway area of Scotland, where an estimated 4,000-6,000 hectares/9,884-14,826 acres
of larch were infected (Forestry Commission - Scotland, 2013b.). This spread is believed
to be a result of exceptionally wet and windy conditions in 2012 combined with the virulent
genetic characteristics of the EU2 lineage. As a result, P. ramorum eradication on larch
in Scotland was declared unachievable, causing the Scotland Forestry Commission to
shift to a containment and slow-the-spread program. A proposed “red zone” (or generally
infested area) in Southwest Scotland has been identified, delineating the area where the
only statutory controls are movement of infested timber and bark. Statutory Plant Health
Notices continue to be issued throughout the rest of Scotland, requiring felling or killing
of infected stands of larch and all surrounding larch within 250 meters/820 feet (Forestry
Commission - Scotland, 2013a).

52 International Oaks, No. 25, 2014

 Sudden Oak Death

Management hopes for the future

As the hope for eradication in each region struggling with P. ramorum dwindles, it is
clear that this pathogen is one with which we must learn to live. Containing outbreaks to
those regions currently infested is a primary goal if we are to protect natural resources,
wildlands, and all the tangible and intangible benefits they provide. Tools to help
minimize impacts from P. ramorum are relatively limited at this point. Educational
outreach currently provides information to all affected parties on how to implement best
management practices, thereby minimizing risk of artificial movement of the pathogen.
Research into “super host” California bay laurel trees that may harbour disease even in the
driest of years may also prove to be important in understanding and minimizing disease
persistence in California (Eyre et al., 2013). Still even further off is the potential for
disease management through deployment of naturally resistant tanoak stock as Hayden
and others (2013) have identified tanoak traits and seedling families with increased
survivorship and provided a framework to further identify seed parents for restoration.

Conclusions
While California, Oregon, and the UK have conditions unique to each region, such
as climate, host species distribution, and pathogen lineage variation, the eradication
actions in each area fell short of desired objectives. All three projects were conducted
with state-of-the-art detection and treatment methods by capable, dedicated teams, yet,
each program has only managed to slow disease spread while the pathogen continues
to kill trees and expand into new areas. The experience gained from these eradication
attempts has yielded many improvements in invasive species management: improved use
of GIS databases and detection techniques as well as better preparation, coordination,
and cooperation among forest managers, affected industry representatives, and regulatory
agency personnel. But it has also demonstrated that complete eradication is likely not
achievable as the pathogen is not identifiable early enough, leading to incomplete disease
delimitation.
Unfortunately, throughout the 20th century similar scenarios have unfolded in Europe
and North America with introductions of white pine blister rust (Cronartium ribicola A.
Dietr.) (Liebhold et al., 2012), chestnut blight (Cryphonectria parasitica (Murrill) Barr)
(Freinkel, 2007), Dutch elm disease (Ophiostoma ulmi (Buisman) Nannf., Ophiostoma
novo-ulmi Brasier) (Brasier, 1991), and other destructive forest pathogens. On average,
two significant invasive forest pests are introduced into the US annually (Aukema et
al., 2010). In Europe, invasive forest pathogens have increased exponentially in the
last four decades, with approximately 60 pathogens introduced from the 1800s to the
present (Santini et al., 2013). If society wants to protect trees, plants, natural resources,
and industries from invasive species, additional ornamental nursery and forest research
is needed to develop new approaches and technologies to prevent their introduction.
Planning and action to protect against the next unknown pathogen is key to sustaining
forests.

Photographers. Title page: Tom Coleman (dying tanoaks). Photo 1: Paul Tooley, USDA Agricultural
Research Service. Photo 3: Tom Coleman, USDA Forest Service, Forest Health Protection. Photo 5:
Ellen Goheen, USDA Forest Service.

International Oaks, No. 25, 2014 53

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For more information about Sudden Oak Death, please visit the California Oak Mortality
Task Force website at hhtp://www.suddenoakdeath.org

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